conifer abundance and its environmental correlates
The abundance of conifers on older terraces was also associated with poor soil drainage, a property that has received little attention from ecosystem ecologists working on chronosequences (but see Mark et al. 1988; Kitayama et al. 1997). Reduced stature on poorly drained soils results from an inability of plants to transport oxygen to deep anchoring roots, without which woody plants are unable to grow tall (Crawford et al. 2003). Lowering the water table on ombrotrophic mires in the northern hemisphere results in aeration of the upper organic layer, and brings about an increase in soil temperature, decomposition rate and nutrient availability (e.g. Silins & Rothwell 1999), all of which facilitate the survival of trees that gradually invade (e.g. Lees 1972; Macdonald & Lin 1999). The prevalence of conifers in waterlogged sites, both in New Zealand and in other temperate forests (Crawford 1987), would appear to result from various morphological and biochemical adaptations. For example, Taxodium distichum develops knee roots containing ventilating tissues that carry oxygen to submerged parts, Pinus species develop large cavities in the steles and Picea species have shallow rooting systems that spread out above the anaerobic region (Crawford 1987). The podocarps on the older terraces were shrubs with many stems, which could improve aeration of roots via aerenchyma (Crawford et al. 2003). In terms of biochemical tolerance to anoxia, little seems to be known about whether conifers have low metabolic rates in their roots or export carbohydrates from their roots (Crawford et al. 2003).
light transmission along the productivity gradient
The difference in light transmission among vegetation types (from ∼1% of incoming PAR on the alluvial forest floor to ∼5% of incoming PAR in terrace forests) is sufficient to have profound effects on seedling survival (Osunkoya et al. 1993; Kobe et al. 1995; Coomes & Grubb 1996; Bloor & Grubb 2003). The few studies of shade tolerance for New Zealand forest trees suggest light-compensation points of between 1% and 4% (Wardle 1991); in northern temperate forests only a minority of species can maintain a positive carbon balance in less than 2% light (Pacala et al. 1996), depending upon nutrient supply from the soil (Coomes & Grubb 2000).
One possible explanation for the deeper shade cast on fertile soils is that trees allocate more resources to leaves when nutrients are plentiful (Tilman 1988; Huston 1994; Whitehead et al. 2004); this idea requires testing for the Waitutu chronosequence. A second explanation is the presence of subcanopy angiosperm trees (Table 3), which were predominantly mesophylls (sensuRaunkiaer 1934; Richardson et al. 2004). A third explanation for differences in light transmission was the presence of tall, dense ferns on the relatively fertile soils, giving way to shorter, less dense ferns on the nutrient-poor soils (Fig. 4, Table 3). Ferns dominate the ground layer in many New Zealand rain forests, particularly where soils and air are reliably moist (Lehmann et al. 2002), and their shade tolerance allows them to persist under evergreen canopies, unlike many herbs in temperate deciduous forests that take advantage of light penetrating to the floor before trees flush their leaves in spring (Ellenberg 1988). The height of ferns across the vegetation types was closely associated with P availability: tree-ferns dominate in P-rich patches of the alluvial forests, and tall Blechnum discolor dominate on older alluvial surfaces, both of which cast deep shade, whereas ferns were much shorter on the terraces, and had highly dissected fronds, which intercepted little light. Similarly, trees ferns are replaced by much shorter ferns on P-limited older sites in Hawaii (Vitousek 2004). The trends toward smaller ground-layer plants is consistent with patterns recorded for bamboos in South America (Veblen 1989) and south-east Asia (Takahashi 1997), whereas a scarcity of herbs is a general feature of infertile soils, both in the tropics (Gentry & Emmons 1987; Coomes & Grubb 1996) and in northern temperate forests (Grubb 1987; Cornwell & Grubb 2003). Herbs proliferate in clearings on fertile soils in North America and Europe, where they grow more quickly than tree seedlings because they invest more resources into resource-capturing tissue and less into structural tissues (Tilman 1982; Bond 1989), but are less abundant in gaps on infertile soils (Ellenberg 1988; Gilliam & Roberts 2003; de Grandpréet al. 2003).
seedling establishment patterns–hares, tortoises and crocodiles
The seminal work of Bond (1989) recognized the importance of resource competition in determining the geographical displacement of conifers, and built a case for conifers being excluded from productive sites because of their relatively slow growth as seedlings. We suggest that conifers in New Zealand are further disadvantaged in relatively productive habitats by three additional mechanisms: (i) shading in the forest understorey is so deep as to prevent shade-tolerant conifers from escaping competition from angiosperms, (ii) ground-ferns restrict seedlings to raised surfaces and (iii) tree-ferns provide sites for angiosperm seedlings to establish.
Firstly, few seedlings of any species were found to establish in the understorey of alluvial forests, presumably because establishment was blocked by shading from the multilayered forest canopy, dense tree-fern layer and near continuous cover of Blechnum discolor (Fig. 4). In contrast, a substantial seedling bank was found in terrace forests (Fig. 6a). Such seedling banks provide shade-tolerant species with a competitive advantage by allowing them to accrue height slowly in the absence of gap formation; this initial height advantage can be critically important when it comes to competition with faster growing seedlings in tree-fall gaps (Canham 1989; Burns 1993; Tanner et al. in press), particularly in fertile soils when competition for light is intense (Keddy et al. 1997). Several conifer species are tolerant of deep shade, but our results suggest that the limited opportunities for seedling-bank formation in the nutrient-rich sites may disadvantage shade-tolerant tree species, both angiosperm and conifer, pushing the system in favour of tree species whose seedlings grow relatively rapidly on logs in tree-fall gaps.
Secondly, seedlings fail to regenerate through the dense ferns on the ground in the alluvial forests, even in tree-fall gaps where herb cover becomes even greater (Midgley et al. 1995; George & Bazzaz 2003): this blocking effect of ferns might disadvantage conifers because of their relatively large seed sizes. In the alluvial forests, hardly any seedlings established under ferns, and seedling densities were 22 times greater on raised surfaces (> 80 cm) than on the forest floor. Small-seeded species produce many more seeds than larger-seeded species (Rees 1995; Coomes & Grubb 2003), and thereby have a greater seed rain onto the few raised surfaces available for establishment. Small-seeded angiosperms require raised surfaces for establishment, as shown by the three smallest seeded species regenerating preferentially on logs in terrace forest (Table 3), whereas all the larger-seeded species (including conifers) were equally able to regenerate on the ground (and would therefore be more affected by microsite restriction). Similar results are reported from Chilean forests, possibly because raised surfaces provide litter-free sites for the establishment of small seedlings, and provide a good substrate for root penetration (Christie & Armesto 2003; Lusk & Kelly 2003). Ground-layer plants can have profound effects on forest dynamics, as illustrated by Takahashi's (1997) work on two conifer species in northern Japan; Abies sachalinensis regenerates on both the ground and elevated sites, and dominates forests in which bamboo is scarce, whereas Picea glehnii regenerates mostly on raised surfaces, and dominates in forests with dense bamboo understories. By analogy, we speculate that podocarps are disadvantaged by dense fern cover in the relatively fertile lowland forests of New Zealand, contributing to their scarcity.
Thirdly, tree-ferns acted as a filter on regeneration by allowing only small-seeded angiosperms to establish on their trunks. About 12% of all seedlings in the alluvial sites were situated on these trunks. Establishing on a vertical surface must present challenges for seedlings, and this is presumably a reason why the small seeds of Weinmannia preferentially establish there, whereas larger-seeded podocarps are absent. Several other studies from New Zealand have noted the importance of tree-fern stems as microsites for the establishment of small-seeded species (Pope 1926; Wardle 1966; Veblen & Stewart 1980). Beveridge (1973) envisaged tree-ferns as a serial species that came to dominate early successional stands, blocking conifer regeneration while allowing epiphytic regeneration of the various angiosperm species which eventually overtopped and suppressed the tree-ferns. In Jamaica, Newton & Healey (1989) have also found that small-seeded Clethra occidentalis relies locally on Cyathea pubescens stems as a site for regeneration.
The filtering effects of ferns in the New Zealand forests are less subtle than those reported by George & Bazzaz (1999a, 1999b, 2003) for forests in north-eastern USA. They showed that ferns reduced the regeneration success of seedlings, and found that some tree species were more affected than others, leading them to propose that the patchiness of fern cover was responsible for spatial heterogeneity in tree regeneration success, with potentially important implications for species coexistence. In contrast, we found that tall ferns formed a nearly continuous cover in the alluvial forests of New Zealand, and that very few seedlings could regenerate through this fern layer. We suggest that the filtering effect of ferns results primarily from the differential ability of tree species to establish on raised surfaces, rather than their differential ability to establish within different fern patches. However, we note that most of the seedlings found on the alluvial forest floor were of Carpodetus serratus, Coprosma foetidissima or Pseudowintera colorata, and that these short tree species are occasionally observed to recruit successfully through the Blechnum layer (i.e. a filtering effect as envisaged by George & Bazzaz 1999a).
The argument that regeneration opportunities for conifers are often more restricted in relatively productive sites is supported by a number of previous studies (Read & Hill 1988; Veblen et al. 1995). In the Andes, Araucaria araucana (Araucariaceae) is able to establish under open canopies of Nothofagus antarctica, which resprouts after fire in drier areas (Burns 1993; Veblen et al. 1995). However, in the more mesic Chilean forests, Araucaria seedlings do not establish under closed stands of N. antarctica or N. dombeyi, but rely on large tree-fall gaps (Veblen 1982). Similarly, A. araucana grows under N. antarctica or N. dombeyi in relatively open Argentinian forests, taking advantage of small gaps as they arise (Burns 1993), but opportunities for regeneration are more limited on mesic sites where N. dombeyi grows faster and forms a denser canopy (Veblen et al. 1995). Fitzroya cupressoides seedlings are commonly found in the understorey of forests in Chilean mountains, but at lower altitudes in Chile they are less frequent at lower altitudes, and are increasingly restricted to areas of large disturbance (Donoso et al. 1993; Veblen et al. 1995). The same observation has been made for podocarps in South Africa (Midgley et al. 1995) and Tasmania (Read & Hill 1988). Together, these various strands of evidence suggest that competition from ground-layer herbs and ferns reduces regeneration opportunities in relatively productive habitats, and contributes to the relatively low abundance of conifers in such habitats.